Physical traits and fitness of cold-induced lethargic Diachasmimorpha longicaudata (Hymenoptera: Braconidae) adults

References

• Alvarenga, C. D., Brito, E. S., Lopes, E. N., Silva, M. A., Alves, D. A., Mantragolo, C. A., & Zucchi, R. A. (2005). Introdução e recuperação do parasitóide exótico Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) em pomares comerciais de Goiaba no Norte de Minas Gerais. Neotropical Entomology, 34(1), 133–136 (in Portuguese with English abstract). https://doi.org/10.1590/S1519-566X2005000100020
   Google Scholar
• Andress, E., Jones, E., War, M., & Shelly, T. (2012). Effects of pre-release chilling on the flight ability of sterile males of the Mediterranean fruit fly (Diptera: Tephritidae). Florida Entomologist, 95(3), 587–592. https://doi.org/10.1653/024.095.0308
   Web of Science ®Google Scholar
• Arredondo, J., Ruiz, L., Hernández, E., Montoya, P., & Díaz-Fleischer, F. (2016). Comparison of Anastrepha ludens (Diptera: Tephritidae) bisexual and genetic sexing (Tapachula-7) strains: Effect of hypoxia, fly density, chilling period, and food type on fly quality. Journal of Economic Entomology, 109(2), 572–579. https://doi.org/10.1093/jee/tov350
   PubMed Web of Science ®Google Scholar
• Baeza-Larios, G., Sivinski, J., Holler, T., & Aluja, M. (2002). The effects of chilling on the fecundity and life span of mass-reared parasitoids (Hymenoptera: Braconidae) of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Biocontrol Science and Technology, 12(2), 205–215. https://doi.org/10.1080/09583150120124469
   Web of Science ®Google Scholar
• Bale, J. (1996). Insect cold hardiness: A matter of life and death. European Journal of Entomology, 93, 369–382.
   Web of Science ®Google Scholar
• Bale, J. S. (2002). Insects and low temperatures: From molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1423), 849–862. https://doi.org/10.1098/rstb.2002.1074
   PubMed Web of Science ®Google Scholar
• Brzezinski, K., & MacMillan, H. A. (2020). Chilling induces unidirectional solute leak through the locust gut epithelia. Journal of Experimental Biology, 223, 1–9. https://doi.org/10.1242/jeb.215475
   Web of Science ®Google Scholar
• Cancino, J., Leal-Mubarqui, R., Angulo, R., Pérez, C., & Tirado, L. (2020a). Effect of density and lethargy duration in prerelease packaging of the fruit fly (Diptera: Tephritidae) parasitoid, Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Journal of Insect Science, 20(1), 1–7. https://doi.org/10.1093/jisesa/ieaa004
   Web of Science ®Google Scholar
• Cancino, J., López, P., Villalobos, P. L., Hipólito, P., Quintero, J. L., & Mattiacci, L. (2006). Control de calidad en la cría masiva de Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Fundamentos y procedimientos, pp. 20–27 (México (in spanish)).
   Google Scholar
• Cancino, J., Mazariegos, D., Pérez, C., Ayala, A., Díaz-Fleischer, F., Leal-Mubarqui, R., & Angulo, R. (2020b). Pre-release packing and chilling reduce host-searching ability of the parasitoid Diachasmimorpha longicaudata used in the augmentative control of tephritid flies. Entomologia Experimentalis et Applicata, 168(5), 350–359. https://doi.org/10.1111/eea.12913
   Web of Science ®Google Scholar
• Chown, S. L., & Gaston, K. J. (2010). Body size variation in insects: A macroecological perspective. Biological Reviews, 85(1), 139–169. https://doi.org/10.1111/j.1469-185X.2009.00097.x
   PubMed Web of Science ®Google Scholar
• Colinet, H., Hance, T., & Vernon, P. (2006). Water relations, fat reserves, survival, and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae). Environmental Entomology, 35(2), 228–236. https://doi.org/10.1603/0046-225X-35.2.228
   Web of Science ®Google Scholar
• David, J. R., Gibert, P., Pla, E., Petavy, G., Karan, D., & Moreteau, B. (1998). Cold stress tolerance in Drosophila: Analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology, 23(5), 291–299. https://doi.org/10.1016/S0306-4565(98)00020-5
   Web of Science ®Google Scholar
• FAO/IAEA/USDA. (2019). Product quality control for sterile mass-reared and released tephritid fruit flies. International Energy Agency. Version 7, 50–59.
   Google Scholar
• Findsen, A., Andersen, J. L., Calderon, S., & Overgaard, J. (2013). Rapid cold hardening improves recovery of ion homeostasis and chill coma recovery time in the migratory locust, Locusta migratoria. Journal of Experimental Biology, 216, 1630–1637. https://doi.org/10.1242/jeb.081141
   PubMed Web of Science ®Google Scholar
• Gaire, S. K., Biswas, M. J. H., Benelli, M., Rempoulakis, P., Taylor, P. W., & Mainali, B. P. (2021). Effect of chilling on quality control parameters of sterile queensland fruit fly (Diptera: Tephritidae). Journal of Economic Entomology, 114(4), 1674–1680. https://doi.org/10.1093/jee/toab092
   PubMed Web of Science ®Google Scholar
• Garcia, F. R. M., Ovruski, S. M., Suárez, L., Cancino, J., & Liburd, O. E. (2020). Biological control of tephritid fruit flies in the Americas and Hawaii: A review of the use of parasitoids and predators. Insects, 11, 1–32. https://doi.org/10.3390/insects11100662
   Web of Science ®Google Scholar
• Gibbs, A. G. (2002). Lipid melting and cuticular permeability: New insights into an old problem. Journal of Insect Physiology, 48(4), 391–400. https://doi.org/10.1016/S0022-1910(02)00059-8
   PubMed Web of Science ®Google Scholar
• Giron, D., & Casas, J. (2003). Lipogenesis in an adult parasitic wasp. Journal of Insect Physiology, 49(2), 141–147. https://doi.org/10.1016/S0022-1910(02)00258-5
   PubMed Web of Science ®Google Scholar
• Hazel, J. R. (1995). Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annual Review of Physiology, 57(1), 19–42. https://doi.org/10.1146/annurev.ph.57.030195.000315
   PubMedGoogle Scholar
• Hernández, E., Escobar, A., Bravo, B., & Montoya, P. (2010). Chilled packing systems for fruit flies (Diptera: Tephritidae) in the sterile insect technique. Neotropical Entomology, 39(4), 601–607. https://doi.org/10.1590/S1519-566X2010000400021
   PubMed Web of Science ®Google Scholar
• Koštál, V., Korbelová, J., Poupardin, R., Moos, M., & Šimek, P. (2016). Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster. Journal of Experimental Biology, 219(15), 2358–2367. https://doi.org/10.1242/jeb.142158
   PubMed Web of Science ®Google Scholar
• Koštál, V., Vambera, J., & Bastl, J. (2004). On the nature of pre-freeze mortality in insects: Water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Journal of Experimental Biology, 207(9), 1509–1521. https://doi.org/10.1242/jeb.00923
   PubMed Web of Science ®Google Scholar
• Le Lann, C., Roux, O., Serain, N., van Alphen, J. J. M., Vernon, P., & van Baaren, J. (2011). Thermal tolerance of sympatric hymenopteran parasitoid species: Does it match seasonal activity? Physiological Entomology, 36(1), 21–28. https://doi.org/10.1111/j.1365-3032.2010.00758.x
   Web of Science ®Google Scholar
• MacMillan, H. A., Baatrup, E., & Overgaard, J. (2015). Concurrent effects of cold and hyperkalaemia cause insect chilling injury. Proceedings of the Royal Society B: Biological Sciences, 282(1817), 1–8. https://doi.org/10.1098/rspb.2015.1483
   Web of Science ®Google Scholar
• MacMillan, H. A., Findsen, A., Pedersen, T. H., & Overgaard, J. (2014). Cold-induced depolarization of insect muscle: Differing roles of extracellular K+ during acute and chronic chilling. Journal of Experimental Biology, 217, 2930–2938. https://doi.org/10.1242/jeb.107516
   PubMed Web of Science ®Google Scholar
• MacMillan, H. A., & Sinclair, B. J. (2011a). Mechanisms underlying insect chill-coma. Journal of Insect Physiology, 57(1), 12–20. https://doi.org/10.1016/j.jinsphys.2010.10.004
   PubMed Web of Science ®Google Scholar
• MacMillan, H. A., & Sinclair, B. J. (2011b). The role of the gut in insect chilling injury: Cold-Induced disruption of osmoregulation in the fall field cricket, Gryllus pennsylvanicus. Journal of Experimental Biology, 214(5), 726–734. https://doi.org/10.1242/jeb.051540
   PubMed Web of Science ®Google Scholar
• MacMillan, H. A., Williams, C. M., Staples, J. F., & Sinclair, B. J. (2012). Reestablishment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus. Proceedings of the National Academy of Sciences USA, 109(50), 20750–20755. https://doi.org/10.1073/pnas.1212788109
   PubMed Web of Science ®Google Scholar
• Makarova, O. L., & Makarov, K. V. (2006). True bugs (Heteroptera) from Arctic Dolgii Island, the Barents Sea. Entomological Review, 86(4), 423–432. https://doi.org/10.1134/S0013873806040063
   Google Scholar
• Montoya, P., Cancino, J., & Ruiz, L. (2012). Packing of fruit fly parasitoids for augmentative releases. Insects, 3(3), 889–899. https://doi.org/10.3390/insects3030889
   PubMedGoogle Scholar
• Montoya, P., Liedo, P., Benrey, B., Cancino, J., Barrera, J. F., Sivinski, J., & Aluja, M. (2000). Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control, 18(3), 216–224. https://doi.org/10.1006/bcon.2000.0819
   Web of Science ®Google Scholar
• Mubarqui, R. L., Perez, R. C., Kladt, R. A., Lopez, J. L. Z., Parker, A., Seck, M. T., Sall, B., & Bouyer, J. (2014). The smart aerial release machine, a universal system for applying the sterile insect technique. PLoS One, 9(7), 1–9. https://doi.org/10.1371/journal.pone.0103077
   Web of Science ®Google Scholar
• Ndlela, S., Azrag, A. G. A., & Mohamed, S. A. (2021). Determination of temperature thresholds for the parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae), using life cycle simulation modeling: Implications for effective field releases in classical biological control of fruit flies. PLoS One, 16(8), 1–21. https://doi.org/10.1371/journal.pone.0255582
   Web of Science ®Google Scholar
• Olson, D. M., Fadamiro, H., Lundgren, J. G., & Heimpel, G. E. (2000). Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiological Entomology, 25(1), 17–26. https://doi.org/10.1046/j.1365-3032.2000.00155.x
   Web of Science ®Google Scholar
• Olsson, T., MacMillan, H. A., Nyberg, N., Staerk, D., Malmendal, A., & Overgaard, J. (2016). Hemolymph metabolites and osmolality are tightly linked to cold tolerance of Drosophila species: A comparative study. Journal of Experimental Biology, 219, 2504–2513. https://doi.org/10.1242/jeb.140152
   PubMed Web of Science ®Google Scholar
• Ovruski, S., Aluja, M., Sivinski, J., & Wharton, R. (2000). Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews, 5(2), 81–107. https://doi.org/10.1023/A:1009652431251
   Google Scholar
• Ovruski, S. M., & Schliserman, P. (2012). Biological control of tephritid fruit flies in Argentina: Historical review, current status, and future trends for developing a parasitoid mass-release program. Insects, 3(3), 870–888. https://doi.org/10.3390/insects3030870
   PubMedGoogle Scholar
• Poikela, N., Tyukmaeva, V., Hoikkala, A., & Kankare, M. (2021). Multiple paths to cold tolerance: The role of environmental cues, morphological traits and the circadian clock gene vrille. BMC Ecology and Evolution, 21(1), 1–20. https://doi.org/10.1186/s12862-021-01849-y
   PubMedGoogle Scholar
• Pujol-Lereis, L. M., Fagali, N. S., Rabossi, A., Catalá, Á, & Quesada-Allué, L. A. (2016). Chill-coma recovery time, age and sex determine lipid profiles in Ceratitis capitata tissues. Journal of Insect Physiology, 87, 53–62. https://doi.org/10.1016/j.jinsphys.2016.02.002
   PubMed Web of Science ®Google Scholar
• R Core Team. (2022). R: A language and environment for statistical computing. Version 4.3.1. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/
   Google Scholar
• Rivero, A., & West, S. A. (2002). The physiological costs of being small in a parasitic wasp. Evolutionary Ecology Research, 4, 407–420.
   Web of Science ®Google Scholar
• Rojas, R. R., & Leopold, R. A. (1996). Chilling injury in the housefly: Evidence for the role of oxidative stress between pupariation and emergence. Cryobiology, 33(4), 447–458. https://doi.org/10.1006/cryo.1996.0045
   Web of Science ®Google Scholar
• Ruiz, L., Cancino, J., Gómez, E., & Montoya, P. (2009). Evaluación del sistema “adulto frío” en el empaque para liberación de Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), parasitoide de moscas de la fruta. Folia Entomologica Mexicana, 48, 29–42 (in Spanish with English abstract).
   Google Scholar
• Shelly, T. E., Edu, J., & Nishimoto, J. (2013). Chilling and flight ability and mating competitiveness of sterile males of the Mediterranean fruit fly. Journal of Applied Entomology, 137(s1), 11–18. https://doi.org/10.1111/j.1439-0418.2010.01532.x
   Google Scholar
• Sinclair, B. J. (1999). Insect cold tolerance: How many kinds of frozen? European Journal of Entomology, 96, 157–164.
   Web of Science ®Google Scholar
• Suárez, L., Biancheri, M. J. B., Murúa, F., Ordano, M;, Wang, X., Cancino, J;, Garcia, F. R. M., Sánchez, G., Beltrachini, S., Kulichevsky, L. E., & Ovruski, S. M. (2023). Medfly population suppression through augmentative release of an introduced parasitoid in an irrigated multi-fruit Orchard of Central-Western Argentina. Insects, 14(4), 387. https://doi.org/10.3390/insects14040387
   PubMed Web of Science ®Google Scholar
• Tejeda, M. T., Arredondo, J., Pérez-Staples, D., Ramos-Morales, P., Liedo, P., & Díaz-Fleischer, F. (2014). Effects of size, sex and teneral resources on the resistance to hydric stress in the tephritid fruit fly Anastrepha ludens. Journal of Insect Physiology, 70, 73–80. https://doi.org/10.1016/j.jinsphys.2014.08.011
   PubMed Web of Science ®Google Scholar
• Toxopeus, J., & Sinclair, B. J. (2018). Mechanisms underlying insect freeze tolerance. Biological Reviews of the Cambridge Philosophical Society, 93(4), 1891–1914. https://doi.org/10.1111/brv.12425
   PubMed Web of Science ®Google Scholar
• Wharton, R. A., & Gilstrap, F. E. (1983). Key to and status of Opiine Braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s. l. (Diptera: Tephritidae). Annals of the Entomological Society of America, 76(4), 721–742. https://doi.org/10.1093/aesa/76.4.721
   Web of Science ®Google Scholar
• Zavala, J. L., Hernández, E., & Montoya, P. (2020). Empaque y liberación de moscas estériles. En P. Montoya, J. Toledo, & E. Hernández (Eds.), Moscas de la Fruta: fundamentos y procedimientos para su manejo (S y G editores, pp. 499–513). Ciudad de México.
   Google Scholar